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Assessment of Anopheles salivary antigens as individual exposure biomarkers to species-specific malaria vector bites

Zakia M I Ali1, Mahfoud Bakli12, Albin Fontaine1, Nawal Bakkali1, Vinh Vu Hai12, Stephane Audebert3, Yvan Boublik4, Frederic Pagès56, Franck Remoué7, Christophe Rogier18, Christophe Fraisier1 and Lionel Almeras12*

Author Affiliations

1 Unité de recherche en biologie et épidémiologie parasitaires (URBEP) – UMR63 – IFR48, Institut de Recherche Biomédicale des Armées (Armed forces biomedical research institute, IRBA), antenne Marseille, GSBdD de Marseille Aubagne, 111 avenue de la corse, BP 40026, Marseille cedex 02, 13568, France

2 Aix Marseille Université, Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198, Inserm 1095, WHO collaborative center for rickettsioses and other arthropod borne bacterial diseases, Faculté de Médecine, 27 bd Jean Moulin, Marseille cedex 5, 13385, France

3 Marseille Proteomic (MaP), Centre de Recherche en Cancérologie de Marseille (CRCM), INSERM CNRS, Aix-Marseille Université, Institut Paoli-Calmette, 27, boulevard Leï Roure, BP 30059, Marseille cedex 09, 13273, France

4 CNRS/CRBM, UMR5237, Montpellier, F-34293, France

5 Institut de Recherche Biomédicale des Armées (IRBA), antenne Marseille, Unité d’Entomologie Médicale, URMITE UMR 6236, GSBdD de Marseille Aubagne, 111 avenue de la corse, BP 40026, Marseille cedex 02, 13568, France

6 Cire Océan indien, 2bis avenue Georges Brassens, Saint Denis Cedex 9, CS 60050-97408, LA REUNION

7 Laboratoire Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle, UMR 224 CNRS/IRD/UM1, Montpellier, France

8 Institut Pasteur de Madagascar, Ambohitrakely, 101, B.P. 1274, Antananarivo, Madagascar

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Malaria Journal 2012, 11:439  doi:10.1186/1475-2875-11-439

Published: 31 December 2012

Abstract

Background

Malaria transmission occurs during the blood feeding of infected anopheline mosquitoes concomitant with a saliva injection into the vertebrate host. In sub-Saharan Africa, most malaria transmission is due to Anopheles funestus s.s and to Anopheles gambiae s.l. (mainly Anopheles gambiae s.s. and Anopheles arabiensis). Several studies have demonstrated that the immune response against salivary antigens could be used to evaluate individual exposure to mosquito bites. The aim of this study was to assess the use of secreted salivary proteins as specific biomarkers of exposure to An. gambiae and/or An. funestus bites.

Methods

For this purpose, salivary gland proteins 6 (SG6) and 5′nucleotidases (5′nuc) from An. gambiae (gSG6 and g-5′nuc) and An. funestus (fSG6 and f-5′nuc) were selected and produced in recombinant form. The specificity of the IgG response against these salivary proteins was tested using an ELISA with sera from individuals living in three Senegalese villages (NDiop, n = 50; Dielmo, n = 38; and Diama, n = 46) that had been exposed to distinct densities and proportions of the Anopheles species. Individuals who had not been exposed to these tropical mosquitoes were used as controls (Marseille, n = 45).

Results

The IgG responses against SG6 recombinant proteins from these two Anopheles species and against g-5′nucleotidase from An. gambiae, were significantly higher in Senegalese individuals compared with controls who were not exposed to specific Anopheles species. Conversely, an association was observed between the level of An. funestus exposure and the serological immune response levels against the f-5′nucleotidase protein.

Conclusion

This study revealed an Anopheles salivary antigenic protein that could be considered to be a promising antigenic marker to distinguish malaria vector exposure at the species level. The epidemiological interest of such species-specific antigenic markers is discussed.

Keywords:
Anopheles gambiae; Anopheles funestus; Antigenic salivary proteins; SG6; 5′nucleotidase; Exposure biomarkers; Epidemiology